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Predictive Factors of Malaria in Travelers to Areas Where Malaria Is Endemic
Enrique Casalino, MD;
Jacques Le Bras, PhD;
Florence Chaussin, MD;
Anika Fichelle, MD;
Elisabeth Bouvet, PhD
Arch Intern Med. 2002;162:1625-1630.
ABSTRACT
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Background The differentiation of malaria from other causes of fever is difficult.
The development of tools for rapid and specific clinical diagnosis is of paramount
importance for the identification of individuals infected with malaria.
Method A 4-year prospective study to identify the clinical and biological variables
associated with malaria included all patients suspected of having malaria
who presented in the emergency department (ED) of a French hospital.
Results Of 783 patients admitted to the ED with suspected malaria, 145 had positive
findings of a thick smear for Plasmodium species, mainly Plasmodium falciparum (90.3%). In univariate analysis, the following
12 variables were significantly associated with diagnosis of malaria: older
than 30 years, male sex, immigration to France from an area where malaria
is endemic, a visit to sub-Saharan Africa, insufficient antimalaria prophylaxis,
fever, chills, absence of diarrhea, a leukocyte count within the reference
range, thrombocytopenia, and increased lactate dehydrogenase and bilirubin
levels. In multivariate analysis, the factors predictive of malaria included
a visit to sub-Saharan Africa (odds ratio [OR], 7.7; 95% confidence interval
[CI], 2.8-21.3), a temperature of at least 38.5°C (OR, 6.2; 95% CI, 2.8-13.3),
chills (OR, 3.0; 95% CI, 1.4-6.6), thrombocytopenia (OR, 16.5; 95% CI, 7.1-38.3),
and abnormally high total bilirubin levels (OR, 21.5; 95% CI, 6.4-72.5). However,
alone or combined, these features had insufficient sensitivity (95.0%) and
low specificity (55.0%) for the diagnosis of malaria.
Conclusions Malaria should be suspected in all patients presenting with complaints
after travel to an area where malaria is endemic, and these patients should
undergo blood microscopy.
INTRODUCTION
MALARIA IS still a major public health problem in many countries. More
than 90 countries are affected, and more than one third of the world population
is exposed to the risk for contracting malaria.1
The number of cases in the world is estimated at 300 million to 500 million
each year, and the number of deaths at 1.5 million to 2.7 million. Malaria
remains the first cause of death in sub-Saharan Africa, where 90% of all cases
occur.
In the United States, Europe, and Australia, imported cases of malaria
are diagnosed among travelers to areas where the disease is endemic. Such
cases have been increasing worldwide, with more than 16 000 diagnosed
in Europe annually, 5000 of them in France, and more than 1500 cases annually
in the United States.2-5
Rapid diagnosis of malaria is essential for the reduction of morbidity
and mortality. However, clinical diagnosis of malaria is difficult in areas
where malaria is endemic, and malaria is not easily distinguished from other
causes of fever. Some studies have evaluated causes of fever and factors predictive
of malaria in areas where malaria is endemic, mostly in children.6-9
Similarly, in areas where malaria is not endemic, imported malaria may
be missed in 40% to 60% of patients presenting with fever after trips to areas
where malaria is endemic, and the clinical presentation of malaria is often
nonspecific.10-15
To our knowledge, no previous prospective study has evaluated the clinical
variables associated with malaria in this setting. Consequently, the development
of tools for rapid and specific clinical diagnosis is of paramount importance
for the identification of individuals infected with malaria.
The goal of the present study was to assess the value of clinical and
easy available biological variables for the diagnosis of malaria among patients
returning from areas where malaria is endemic.
PATIENTS AND METHODS
SETTING
This study was conducted in the Bichat-Claude Bernard Hospital, a 1300-bed
university-affiliated teaching hospital that serves as a referral center and
primary care facility in the metropolitan area of Paris, France. More than
60 000 patients visit the hospital's emergency department (ED) each year.
PATIENTS
We included all patients presenting to the Bichat-Claude Bernard ED
who underwent laboratory tests for the diagnosis of malaria during the 4 years
from August 1, 1995, through July 31, 1999.
METHODS
Clinical and demographic data were obtained from the patients' medical
charts and from the Parasitology Department. Diagnosis of malaria was obtained
by means of thick- and thin-smear microscopy. Quantitative buffy-coat analysis
was performed overnight and during weekends, but results of thick and thin
smears were obtained in all cases at soon as possible. If these results were
negative, a new parasitological test was performed if clinically indicated.
Optimal prophylaxis was defined as the use of an adequate drug (a combination
of chloroquine diphosphate plus chloroguanide hydrochloride or mefloquine
hydrochloride for patients visiting sub-Saharan Africa) with good compliance
(respect of drug scheduling and dosage) during the stay in the area where
malaria is endemic and 4 weeks after the return to an area where the disease
is not endemic.
To explore the possible relationship between clinical or biological
variables and malaria diagnosis, we used the Kruskal-Wallis 1-way analysis
of variance for continuous variables and the  2 test with the
Fisher 2-tailed exact test for categorical variables. If necessary, continuous
variables were classified by choosing their median or clinically relevant
value. A P value of no greater than .05 was used
to determine statistical significance.
The variables found to be significant and those with a P value of less than .25 by univariate analysis were included in a
logistic regression model and eliminated one by one in a backward fashion
on the basis of the adjusted odds ratio (OR) to develop a model with the strongest
possible relationships. From these results, a prediction model was proposed.
Clinical features at admission and laboratory data were assigned weights based
on the results of the values found by univariate and multivariate analysis
to determine the best predictor of malaria in an individual patient. The sensitivity
and specificity of the model for predicting malaria in the population studied
were determined for each score value. After stratification, the performance
of the malaria prediction model was assessed by means of the receiver operating
characteristics (ROC) curve.
Data are presented as mean ± SD. Median values and ranges are
presented when necessary.
We used Statistica 5.1 (StatSoft, Inc, Tulsa, Okla) and EPI-INFO 6 (World
Health Organization, Geneva, Switzerland) software for data collection and
analysis.
RESULTS
PATIENT CHARACTERISTICS
We included 783 consecutive patients during the 4-year study. Patient
characteristics are given in Table 1.
More than half of the patients were born in regions where malaria is endemic.
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Table 1. Characteristics of 783 Patients Suspected of Having Malaria
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MALARIA PROPHYLAXIS
Malaria prophylaxis was used by 39.0% of the patients, but only 44.9%
of them complied with their treatment while visiting the area where malaria
is endemic and after their return to France; thus, only 17.5% of the entire
population had optimal prophylaxis.
The following factors were associated with good antimalaria prophylaxis:
age ( 30 or >30 years, 31.3% vs 9.7%, respectively [P<.001]); sex (female or male, 25% vs 12.4%, respectively [P = .03]); and patients' origin (area where malaria is
not or is endemic, 30.3% vs 5.8%, respectively [P<.001]).
Differences in prophylaxis use were found according to the following visited
areas: Asia, 45%; sub-Saharan Africa, 18.7%; and North Africa, 0% (P = .01).
MALARIA DIAGNOSIS
Malaria was diagnosed in 145 patients (18.5%). Plasmodium
falciparum was identified in 131 cases (90.3%); Plasmodium ovale, in 8 (5.5%); and
Plasmodium vivax, in 7 (4.8%). One patient had coinfection by P falciparum and
P vivax. Of the 131 patients infected
by P falciparum, 127 contracted their infection in
sub-Saharan Africa (mostly French-speaking west Africa) and the other 4 in
Indonesia, Southeast Asia, or South America. All 8 cases of P ovale infections were contracted in sub-Saharan Africa. The 7 cases
of P vivax infections were contracted in India, Central
America, and north and sub-Saharan Africa. More than 90% of cases of malaria
were acquired in sub-Saharan Africa.
The following diagnoses were assigned to patients in whom malaria was
not detected: febrile diarrhea (12.5%), urinary tract infection (6.2%), lower
respiratory tract infection (9.6%), upper respiratory tract infection (6.8%),
acute meningitis (3.4%), acute hepatitis (2.8%), and cutaneous infection (3.4%);
the remaining patients (55.3%) had fever without any identified cause (except
for 1 patient with an acute Epstein-Barr virus infection).
PREDICTIVE FACTORS OF MALARIA
The clinical and biological features associated with a diagnosis of
malaria are shown in Table 2 and Table 3. Patients with malaria were significantly
older than the others. Most were male and came from areas where malaria is
endemic. More had visited sub-Saharan Africa, and more had received nonoptimal
prophylaxis. Most patients with malaria had a history of fever before arrival
in our ED, presented with chills but not with diarrhea, had fever on arrival
in the ED, and had lower leukocyte and platelet counts and higher lactate
dehydrogenase and bilirubin concentrations.
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Table 2. Comparison of Continuous Variables Between Patients With and
Without Malaria*
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Table 3. Clinical Variables Associated With the Diagnosis of Malaria*
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The results of multivariate analysis (Table 4) disclosed 5 independent factors predictive of malaria:
a visit to sub-Saharan Africa (OR, 7.7; 95% confidence interval [CI], 2.8-21.3);
a temperature of at least 38.5°C on arrival in the ED (OR, 6.2; 95% CI,
2.8-13.3); chills (OR, 3.0; 95% CI, 1.4-6.6); a platelet count below 130 000
cells/µL (OR, 16.5; 95% CI, 7.1-38.3); and total bilirubin levels of
at least 1.05 mg/dL (>18 µmol/L) (OR, 21.5; 95% CI, 6.4-72.5).
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Table 4. Independent Predictive Factors of Malaria Disclosed by Multivariate
Analysis
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Figure 1 presents the scatterplots
of temperature at admission, platelet count, and total bilirubin levels according
to malaria diagnosis. The reference range for total bilirubin level is less
than 1.4 mg/dL (<24 µmol/L). Figure
2 shows the ROC curve for malaria diagnosis according to clinical
variables at admission. Figure 3
shows the ROC curve for clinical and biological variables.
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Figure 1. Scatterplots of temperature (A),
platelet counts (B), and total bilirubin levels (C) according to malaria diagnosis.
Bars indicate range; large boxes, 25th to 75th percentiles; and small boxes,
median values. To convert total bilirubin level from milligrams per deciliter
to micromoles per liter, multiply by 17.1.
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Figure 2. Receiver operating characteristic
curve for the diagnosis of malaria according to clincial features at admission.
The curve includes the following variables: older than 30 years, a visit to
sub-Saharan Africa, inadequate prophylaxis for malaria, fever before arrival
in the emergency department (ED), chills, absence of diarrhea, and temperature
on arrival in the ED of at least 38.5°C. For all variables except the
last one, we used the odds ratio obtained by univariate analysis; for the
last variable, we used the odds ratio obtained by multivariate analysis.
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Figure 3. Receiver operating characteristic
curve for the diagnosis of malaria according to clinical features at admission
and laboratory data. This curve included the clinical variables used in Figure
2, plus thrombocytopenia and high total bilirubin levels. For the 2 new variables,
the odds ratios obtained by multivariate analysis were used to calculate the
final score.
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COMMENT
In the present study, the need for parasitological tests for malaria
was used as the inclusion criterion. We found that these tests had been prescribed
for patients who had returned from areas where malaria is endemic during the
past year and who exhibited nonspecific symptoms such as fever, chills, headache,
myalgia, and abdominal complaints. We found that imported malaria is a frequent
consultation reason in the emergency setting; that P falciparum is the most frequent causative Plasmodium
species in France; that some patients seeking medical care after a visit in
an area where malaria is endemic had not received optimal antimalaria prophylaxis;
and that the diagnosis of malaria remains a clinical difficulty.
Our study included patients with different degrees of immunity to malaria
depending on their origin and, for immigrant non-French patients, their period
of residence in an area where the disease is not endemic. In the present study,
immune and semi-immune immigrant patients, defined as those with a history
of a malaria attack or those born in rural areas where malaria is endemic,
accounted for more than 50% of all patients undergoing testing for malaria
and of those with a diagnosis of malaria, as reported by other authors in
studies of imported malaria.3, 5, 16-23
Despite the large number of patients included, our study population probably
did not correspond to the total number of those traveling to areas where malaria
is endemic. However, it probably corresponded fairly well to the population
of subjects who are symptomatic after a journey to a tropical region and who
live in a large city located in an area where malaria is not endemic. Otherwise,
there are some differences between the patients with malaria identified in
the present study compared with those seen in the United States, where P vivax is more frequent and where a greater number of
cases are acquired outside of Africa.5
An important result of our study was that only 17.5% of the entire population
complied with the currently accepted chemoprophylactic regimens for travelers
in areas where malaria is endemic, which is consistent with previously published
data.10, 17, 19, 21, 24-26
We found that noncompliance with antimalaria chemoprophylaxis was associated
with the immigrants' origin (as previously reported23, 27),
age greater than 30 years, and male sex.
Malaria was diagnosed in 18.5% of the patients in the present study.
Previous reports indicated proportions of 4% to 36%.11, 28 Plasmodium falciparum was identified in 90% of our malaria
cases, and in 10% to 76% by others.5, 11-13,15, 28-29
The areas visited and the world distribution of Plasmodium species are closely related to Plasmodium
strain identification and the proportion of patients with P falciparum.4
The diagnosis of imported malaria remains a challenge for most clinicians.
In industrialized countries, malaria may be initially missed in up to 60%
of patients attending hospital consultations,10-11,13, 15
and the disease is still associated with a high fatality rate.3
Although it is currently accepted that the clinical presentation of malaria
is often nonspecific, some clinical features have been frequently associated
with its diagnosis, especially visits to sub-Saharan Africa,30
thrombocytopenia (reported in 43%-75% of patients with malaria), and increased
bilirubin levels (in 30%-64%).13 Fever is also
frequently associated with malaria, but may be absent in 2.4% to 51% of cases.13, 31-33
The present study includes a very large number of patients with complaints
that may be related to malaria and a large number with a documented diagnosis
of malaria. We found that certain easily available clinical and biological
features may be predictive of the disease. Univariate analysis showed that
the factors significantly associated with the diagnosis of malaria were age
greater than 30 years, male sex, foreign origin, a visit to sub-Saharan Africa,
noncompliance with chemoprophylaxis, a fever before arrival in the hospital,
chills, the absence of diarrhea, a temperature of at least 38.5°C, a leukocyte
count within the reference range, thrombocytopenia, and mild elevation of
lactate dehyrogenase and bilirubin levels. However, the positive and negative
predictive values of these factors were low.
Although we found, on multivariate analysis, that a visit to sub-Saharan
Africa, a temperature of at least 38.5°C, chills, thrombocytopenia, and
high total bilirubin levels were independent predictors of malaria, these
signs were not sufficiently sensitive or specific to differentiate malaria
from other diseases. In addition, ROC curves showed that, alone or in combination,
these features were not sensitive or specific enough to permit the diagnosis
of malaria. Our data are consistent with the results of a previous report
on the diagnosis of malaria in travelers.34
When the ROC curves in Figure 1
and Figure 2 were compared, laboratory
tests for thrombocytopenia and high total bilirubin levels displayed poor
sensitivity gain but greater specificity.
Consequently, we believe that, if on arrival in the hospital or in a
prehospital setting, a visit to sub-Saharan Africa, absence of prophylaxis
for malaria, fever (especially high fever), and chills are present, a diagnosis
of malaria should be considered, and patients should undergo testing for malarial
parasites. On the other hand, if biological features such as thrombocytopenia
or increased bilirubin levels are found, malaria should be suspected, patients'
characteristics should be reevaluated, and parasitological tests for malaria
should be prescribed if the subject has a history of travel to an area where
malaria is endemic.
CONCLUSIONS
Malaria remains a challenge for clinicians. According to past and present
data, all symptomatic patients with a history of travel to an area where malaria
is endemic should undergo microscopic examination or testing for a rapid diagnosis
of malaria. Certain clinical and laboratory features may be predictive of
malaria, but their sensitivity and specificity are insufficient. Our results
strongly suggest that patients who return from areas where malaria is endemic
and who present with clinical and biological variables suggestive of malaria
but with negative findings of a blood film test should undergo clinical and
parasitological reevaluation to exclude a diagnosis of malaria.
AUTHOR INFORMATION
Accepted for publication November 20, 2001.
Corresponding author and reprints: Enrique Casalino, MD, Service
d'Accueil des Urgences, 78, rue du Général Leclerc, 94275 Le
Kremlin Bicêtre CEDEX, France (e-mail: enrique.casalino{at}bct.ap-hop-paris.fr).
From the Emergency Department (Drs Casalino, Chaussin, and Fichelle),
the Infectious and Tropical Diseases Unit A (Drs Casalino and Bouvet), and
the Laboratory of Parasitology and Centre National de Référence
pour la Chimiosensibilité du Paludisme (Dr Le Bras), Bichat-Claude
Bernard University Hospital, Paris, France. Dr Casalino is now with the Service
d'Accueil des Urgences, Hôpital Universitaire de Bicêtre, Bicêtre,
France.
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